Maternal cortisol level around conception is associated with offspring sex ratio in captive European wild rabbit (Oryctolagus cuniculus)

Szerzők

  • Benedek Ildikó Magyar Agrár- és Élettudományi Egyetem (MATE) Kaposvári Campus
  • Altbäcker Vilmos Magyar Agrár- és Élettudományi Egyetem (MATE) Kaposvári Campus
  • Zsolnai Attila Magyar Agrár- és Élettudományi Egyetem (MATE) Kaposvári Campus https://orcid.org/0000-0002-8382-1503
  • Molnár Tamás Magyar Agrár- és Élettudományi Egyetem (MATE) Kaposvári Campus https://orcid.org/0000-0003-1752-4268

DOI:

https://doi.org/10.31914/aak.2793

Kulcsszavak:

sex allocation, stress, progesterone, glucocorticoids, faecal cortisol

Absztrakt

The sex ratio of the offspring at birth is usually 1: 1 established by natural selection. The sex allocation model predicts that if parents have adequate resources, they would benefit from differentially allocating maternal investment to that sex having higher fittness under the particular environmental conditions. However, little is known about what mechanisms would result in biased sex ratio. One such mechanism could be the interaction of of stress reactivity and progesterone levels in the mothers around conception. In the present investigation the fecal cortisol and progesterone levels at the day of conception were measured in fifteen European wild rabbit does kept in cages. The does were clustered to low and high cortisol response groups and the sex ratio of their progeny was determined. We found a significant correlation between the progesterone levels of mothers and their stress status measured at the mating. This correlation was also reflected in the sex ratio bias in their litters. Even though the litter size was not different, we found higher progesterone levels and more female offspring in the does with higher cortisol levels indicating that maternal status around conception may affect the litter sex ratio.

Hivatkozások

Albrecht, E. D., Nightingale, M. S., Townsley, J. D. (1978). Stress-induced decreases in the serum con-centration of progesterone in the pregnant baboon. J Endocrino., 77(3), 425–426. DOI: https://doi.org/10.1677/joe.0.0770425

Bánszegi, O., Altbäcker, V., Bilkó, Á. (2009). Intrauterine position influences anatomy and behavior in domestic rabbits. Physiol Behav., 98(3), 258–262. DOI: https://doi.org/10.1016/j.physbeh.2009.05.016

Beaulieu-McCoy, N.E., Sherman, K. K., Trego, M. L., Crocker, D.E., Kellar, N.M., (2017). Initial validation of blubber cortisol and progesterone as indicators of stress response and maturity in an otariid; the California sea lion (Zalophus californianus). Gen Comp Endocr.; 252, 1–11. DOI: https://doi.org/10.1016/j.ygcen.2017.07.003

Benedek, I., Altbӓcker, V., Molnár, T. (2021). Stress reactivity near birth affects nest building timing and offspring number and survival in the European rabbit (Oryctolagus cuniculus). Plos one, 16(1), e0246258. DOI: https://doi.org/10.1371/journal.pone.0246258

Bilkó, Á.; Altbäcker V.(2000). Regular handling early in the nursing period eliminates fear responses toward human beings in wild and domestic rabbits. Dev. Psychobiol., 36, 78–87. DOI: https://doi.org/10.1002/(SICI)1098-2302(200001)36:1<78::AID-DEV8>3.0.CO;2-5

Breazile, J. E. (1988). The physiology of stress and its relationship to mechanisms of disease and therapeutics. Vet Clin N A.-Food A., 4(3), 441–480. DOI: https://doi.org/10.1016/S0749-0720(15)31025-2

Cabezas S, Blas J, Marchant T.A, Moreno S. (2007). Physiological stress levels predict survival proba-bilities in wild rabbits. Horm Behav. 51(3), 313–320. DOI: https://doi.org/10.1016/j.yhbeh.2006.11.004

Cameron, E. Z. (2004). Facultative adjustment of mammalian sex ratios in support of the Trivers–Willard hypothesis: evidence for a mechanism. ProcRoyal SocB: Biol Sci, 271(1549), 1723–1728. DOI: https://doi.org/10.1098/rspb.2004.2773

Chandler, J. E., Canal, A. M., Paul, J. B., Moser, E. B. (2002). Collection frequency affects percent Y-chromosome bearing sperm, sperm head area and quality of bovine ejaculates. Theriogenology, 57(4), 1327–1346. DOI: https://doi.org/10.1016/s0093-691x(01)00721-x

Charnov, E.L. (1983) The theory of sex allocation. Princeton University Press, Princeton. DOI: https://doi.org/10.1515/9780691210056

Clutton-Brock, T. H., Albon, S. D., Guinness, F. E. (1984). Maternal dominance, breeding success and birth sex ratios in red deer. Nature, 308(5957), 358–360. DOI: https://doi.org/10.1038/308358a0

Clutton-Brock, T. H., Guinness, F. E., & Albon, S. D. (1982). Red deer: behavior and ecology of two sexes. University of Chicago press, Chicago.

Coubrough, R. I. (1985). Stress and fertility. Onderstepoort J Vet., 52, 153–156. URI: http://hdl.handle.net/2263/44393

Desfor, K. B., Boomsma, J. J., Sunde, P. (2007). Tawny owls Strix aluco with reliable food supply pro-duce male‐biased broods. Ibis, 149(1), 98–105. DOI: https://doi.org/10.1111/j.1474-919x.2006.00617.x

Edwards, A. M., Cameron, E. Z. (2014). Forgotten fathers: paternal influences on mammalian sex allocation. Trends Ecol Evol., 29(3), 158-164. DOI: https://doi.org/10.1016/j.tree.2013.12.003

Emlen, S. T., Emlen, J. M., Levin, S. A. (1986). Sex-ratio selection in species with helpers-at-the-nest. Am Nat., 127, 1-8.

Fajer, A. B., Holzbauer, M., Newport, H. M. (1971). The contribution of the adrenal gland to the total amount of progesterone produced in the female rat. J Physiol., 214(1), 115–126. DOI: https://doi.org/10.1113/jphysiol.1971.sp009422

Fisher, R. A. (1930): 117ze Genetical Theory of Natural Selection. Clarendon Press, Oxford.

Grant, V. J. (2007). Could maternal testosterone levels govern mammalian sex ratio deviations?. J Theor Biol., 246(4), 708–719. DOI: https://doi.org/10.1016/j.jtbi.2007.02.005

Grant, V. J., Irwin, R. J. (2005). Follicular fluid steroid levels and subsequent sex of bovine embryos. J Exp Zool Part A., 303(12), 1120–1125. DOI: https://doi.org/10.1002/jez.a.233

Gutiérrez‐Adán, A., Perez‐Crespo, M., Fernandez‐Gonzalez, R., Ramirez, M. A., Moreira, P., Pintado, B., Rizos, D. (2006). Developmental consequences of sexual dimorphism during pre‐implantation embryonic development. Reprod Domest Anim., 41, 54–62. DOI: https://doi.org/10.1111/j.1439-0531.2006.00769.x

Hamilton, W. D. (1967). Extraordinary Sex Ratios: A sex-ratio theory for sex linkage and inbreeding has new implications in cytogenetics and entomology. Science, 156, 477–488.

Henriksen, T. B., Wilcox, A. J., Hedegaard, M., Secher, N. J. (1995). Bias in studies of preterm and post-term delivery due to ultrasound assessment of gestational age. Epidemiology, 6(5), 533-537. DOI: https://doi.org/10.1097/00001648-199509000-00012

Howe, H. F. (1977). Sex-ratio adjustment in the common grackle. Science, 198 (4318), 744–746. DOI: https://doi.org/10.1126/science.198.4318.744

James, W. H. (2004). Further evidence that mammalian sex ratios at birth are partially controlled by parental hormone levels around the time of conception. Hum Reprod., 19(6), 1250–1256. DOI: https://doi.org/10.1093/humrep/deh245

James, W. H. (2006). Possible constraints on adaptive variation in sex ratio at birth in humans and other primates. J Theor Biol., 238(2), 383–394. DOI: https://doi.org/10.1016/j.jtbi.2005.05.022

Jongbloet, P. H. (2004). The ovopathy concept for explaining the secondary sex ratio. Hum Reprod., 19(4), 1036–1037. DOI: https://doi.org/10.1093/humrep/deh140

Komdeur, J. (2004). Sex-ratio manipulation. Ecology and evolution of cooperative breeding in birds. Cambridge University Press, Cambridge, 102-116.

Komdeur, J. (2012). Sex allocation. The evolution of parental care, In: N J. Royle, PT. Smiseth, MKölli-ker (Eds.), Oxford University Press, Oxford, UK, 171-188.

Korsten, P., Clutton-Brock, T., Pilkington, J. G., Pemberton, J. M., Kruuk, L. E. (2009). Sexual conflict in twins: male co-twins reduce fitness of female Soay sheep. Biol Letters, 5(5), 663–666. DOI: https://doi.org/10.1098/rsbl.2009.0366

Larson, M. A., Kimura, K., Kubisch, H. M., Roberts, R. M. (2001). Sexual dimorphism among bovine embryos in their ability to make the transition to expanded blastocyst and in the expression of the signaling molecule IFN-τ. Proc Natl Acad Sci-Biol., 98(17), 9677–9682. DOI: https://doi.org/10.1073/pnas.171305398

Lessells, C. M., Avery, M. I. (1987). Sex-ratio selection in species with helpers at the nest: some exten-sions of the repayment model. Am Nat., 129(4), 610–620.

Marcus, M., Kiely, J., Xu, F., McGeehin, M., Jackson, R., Sinks, T. (1998). Changing sex ratio in the United States, 1969–1995. Fertil Steril., 70(2), 270–273. DOI: https://doi.org/10.1016/s0015-0282(98)00149-6

McMillen, M. M. (1979). Differential mortality by sex in fetal and neonatal deaths. Science, 204(4388), 89–91. DOI: https://doi.org/10.1126/science.571144

Obel, C., Henriksen, T. B., Secher, N. J., Eskenazi, B., Hedegaard, M. (2007). Psychological distress during early gestation and offspring sex ratio. Hum Reprod., 22(11), 3009–3012. DOI: https://doi.org/10.1093/humrep/dem274

Palmer, A. R. (2000). Quasi-replication and the contract of error: lessons from sex ratios, heritabili-ties and fluctuating asymmetry. Annu Rev Ecol Syst., 31(1), 441–480. DOI: https://doi.org/10.1146/annurev.ecolsys.31.1.441

Pongrácz, P.; Altbäcker, V.; Fenes, D. (2001). Human handling might interfere with conspecific recog-nition in the European rabbit (Oryctolagus cuniculus). Dev. Psychobiol., 39(1), 53–62. DOI: https://doi.org/10.1002/dev.1028

Pratt, N. C., Lisk, R. D. (1989). Effects of social stress during early pregnancy on litter size and sex ratio in the golden hamster (Mesocricetus auratus). Reproduction, 87(2), 763–769. DOI: https://doi.org/10.1530/jrf.0.0870763

Rivers, J. P. W., Crawford, M. A. (1974). Maternal nutrition and the sex ratio at birth. Nature, 252(5481), 297–298.

Rosenfeld, C. S., Roberts, R. M. (2004). Maternal diet and other factors affecting offspring sex ratio: a review. Biol Reprod., 71(4), 1063–1070. DOI: https://doi.org/10.1095/biolreprod.104.030890

Ryan, C. P., Anderson, W. G., Berkvens, C. N., Hare, J. F. (2014). Maternal gestational cortisol and testosterone are associated with trade-offs in offspring sex and number in a free-living rodent (Urocitellus richardsonii). PloS one, 9(10), e111052. DOI: https://doi.org/10.1371/journal.pone.0111052

Sheldon, B. C., West, S. A. (2004). Maternal dominance, maternal condition, and offspring sex ratio in ungulate mammals. Am Nat., 163(1), 40–54. DOI: https://doi.org/10.1086/381003

Teixeira, C. P., De Azevedo, C. S., Mendl, M., Cipreste, C. F., Young, R. J. (2007). Revisiting translocation and reintroduction programmes: the importance of considering stress. Anim Behav., 73(1), 1–13. DOI: https://doi.org/10.1016/j.anbehav.2006.06.002

Trivers, R. L., Willard, D. E. (1973). Natural selection of parental ability to vary the sex ratio of offspring. Science, 179(4068), 90–92. DOI: https://doi.org/10.1126/science.179.4068.90

Weatherhead, P. J., Robertson, R. J. (1979). Offspring quality and the polygyny threshold:" the sexy son hypothesis". Am Nat., 113(2), 201–208. DOI: https://doi.org/10.1086/283379

West, S. A., Sheldon, B. C. (2002). Constraints in the evolution of sex ratio adjustment. Science, 295(5560), 1685–1688. DOI: https://doi.org/10.1126/science.1069043

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Megjelent

2022-07-29

Hogyan kell idézni

Benedek, I., Altbäcker, V., Zsolnai, A., & Molnár, T. (2022). Maternal cortisol level around conception is associated with offspring sex ratio in captive European wild rabbit (Oryctolagus cuniculus). Acta Agraria Kaposváriensis, 26(1), 7–16. https://doi.org/10.31914/aak.2793

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